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International Standards for Research Integrity: An Idea Whose Time has Come?

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A movement to promulgate international ethics standards covering areas of conduct other than research with human subjects has now begun to gain momentum. This commentary explains why it is important to develop international research integrity standards and some of the problems that must be overcome to bring them to fruition.
Vol. 5, No. 9, September 2009 “Can You Handle the Truth?”
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International Standards for Research Integrity:
An Idea Whose Time has Come?
By David Resnik
This article is reprinted from Accountability in Research, 16:4, 218-228
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Abstract
A movement to promulgate international ethics standards covering areas of conduct other
than research with human subjects has now begun to gain momentum. This commentary
explains why it is important to develop international research integrity standards and some
of the problems that must be overcome to bring them to fruition.
Introduction
Research integrity encompasses a wide range of topics relating to the ethical conduct of
research, including research involving human and animal subjects, research design, data
management, data analysis, data fabrication/falsification, publication, authorship,
plagiarism, peer review, mentoring, science-industry relationships, conflict of interest,
intellectual property, and social responsibility (Steneck, 2007, Shamoo and Resnik, 2009).
Scientific research is truly global in scope, with international collaborations, conferences,
journals, databases and so on. Although science transcends national boundaries, with the
exception of research involving human subjects, there are no definitive international
standards for research integrity.
International standards for the ethical conduct of research with human subjects have been
in place since the adoption of the Nuremberg Code after the end of World War II
(Nuremberg Code, 1949). The Code was adopted by the Nuremberg Military Tribunal to
judge Nazi physicians and scientists accused of war crimes committed against concentration
camp prisoners used in human experiments. Before this time, some investigators, such as
William Osler and Claude Bernard, had written about the ethics of clinical research; some
countries, such as the region of Prussia, had adopted rules for research with human
subjects, and some professional organizations, such as the American Medical Association,
were in the process of developing guidelines, but it took the horrific acts committed by the
Nazis to convince the world community of the need for international standards for research
with human subjects (Shamoo and Resnik, 2009). Other guidelines have been adopted in
the years following the development of the Nuremberg Code. In 1964, the World Medical
Association (WMA) adopted its Helsinki Declaration, and in 1982 the Council for the
International Organization of Medical Sciences (CIOMS) developed its guidelines (WMA,
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1964; CIOMS, 2002). Both documents have been revised many times since they were first
adopted.
A movement to promulgate international ethics standards covering areas of conduct other
than research with human subjects has only now begun to gain momentum. From
September 16 to 19, 2007, in Lisbon, Portugal, the Office of Research Integrity (ORI) and
European Science Foundation (ESF) convened the first global forum on research integrity.
The goal of the conference was to assemble researchers, administrators, sponsors, editors,
policymakers and other people from around the globe to discuss ways of harmonizing
misconduct policies and fostering ethical research (Mayer and Steneck, 2007). The Co-
Chairs of the conference, Tony Mayer and Nicholas Steneck, recommended that ORI and
ESF work with the Global Science Forum (GSF) and the Organization for Economic
Cooperation and Development (OECD) in promoting international research cooperation on
research integrity. They recommended that these organizations should work together to
“clarify, harmonize, and publicize standards for best practices and procedures for reporting
improper conduct in research” (Mayer and Steneck, 2007).
Long before the ORI and ESF organized this conference, journal editors from around the
world had collaborated on some ethical standards dealing with research integrity. For
example, the International Committee of Medical Journal Editors (ICMJE) has ethical
standards dealing with authorship, conflict of interest, and protection of human and animal
subjects. Seven hundred journals follow the ICMJE standards (ICMJE, 2008). The
Committee on Publication Ethics (COPE), an organization that promotes integrity in peer-
reviewed scientific publications, has ethical standards pertaining to research misconduct,
peer review, authorship, redundant publication, conflict of interest, data analysis, and
protecting human and animal subjects. Over 3,800 journals belong to COPE (COPE, 2009).
A recent, high-profile case involving research misconduct has brought the need for
international research integrity standards into sharp relief. In 2004 and 2005, Seoul
University researcher Woo-Suk Hwang and colleagues published two articles in the journal
Science reporting the derivation of HES cell lines by therapeutic cloning. Hwang received
international recognition for his work and became a national hero. In November 2005,
University of Pittsburgh scientist Gerald Schatten, who collaborated with Hwang on the 2005
article, accused Hwang of misleading members of the research team about the sources of
human oocytes used in the research. Hwang admitted that some of the oocytes came from
women working in his lab, which was not illegal in South Korea, but was ethically
questionable. The women were paid $1400 for their eggs. In December 2005, the editors of
Science received an anonymous tip that two of the photo cell lines in the 2005 article were
duplications. Later, one of Hwang's co-authors, Sung Roh, told the media that Hwang had
fabricated 9 of the 11 cell lines presented in the article. Hwang asked for the article to be
withdrawn from Science, and a committee from Seoul University began investigating the
2005 article and Hwang's other publications.
Hwang resigned his position at Seoul University at the end of December 2005. In May 2006,
Hwang and five collaborators were indicted on charges of fraud, embezzlement ($3 million),
and breach of bioethics laws. Schatten was never accused of fabricating data, but a
committee at his university found that he had shirked his authorship responsibilities and
accepted excessive consulting fees ($40,000) for collaborating with Hwang over an 18-
month period (Resnik, et al. 2006, Saunders and Savulescu, 2008).
International standards for research integrity are important for several reasons. First,
because research is often international in scope, it is necessary to have ethical standards
that transcend national boundaries to resolve disputes that may arise when the parties
come from different countries. For example, suppose that a reviewer from country A
suspects that an article submitted by authors from country B plagiarizes a previously
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published article from country A. Suppose, also, that government organizations from
country A and country B have different definitions of plagiarism. The authors could argue
that their behavior does not qualify as plagiarism according to their country's rules. It may
be difficult to resolve this issue without appealing to a common definition.
Second, scientists can appeal to international integrity standards in the absence of local
standards. For example, if a developing nation has no regulations pertaining to data
fabrication or falsification, then international standards could be used to evaluate scientific
conduct. The Helsinki Declaration has functioned as a standard of conduct for research with
human subjects in the absence of local laws (Brody, 1998).
Third, well-recognized, clear and coherent international integrity standards can encourage
the development of local standards. Countries that lack local standards for the conduct of
research can use international standards as a model for the development of their own rules
and policies. Some countries have used the Helsinki Declaration as a guide to developing
their own policies, for example (Brody, 1998).
Fourth, international standards for research integrity can foster trust among scientists
working in different countries. Investigators who are planning an international collaboration
appeal to international standards as a benchmark for authorship, publication, data sharing,
and other important concerns. If an ethical dispute arises during the collaboration, the
investigators can appeal to a common benchmark.
Though there is clearly an urgent need for international research integrity standards,
several difficulties must be overcome to bring them to fruition. The first difficulty is to
ensure that the organization(s) sponsoring the standards have sufficient influence to gain
the attention of a large percentage of scientists around the world. The organizations that
developed the Nuremberg Code and the Helsinki Declaration had considerable clout. The
Nuremberg Military Tribunal, convened by the Allied Powers at the end of World War II,
commanded the attention of the entire world as it passed judgment on Nazi war crimes. The
WMA, which was founded in 1947, includes representatives from national medical
associations from 85 countries. The WMA has held annual meetings since its inception in
countries from Europe, Asia, North America, South America, and Australia (WMA, 2009).
Although the ORI, ESF and OECD have some influence and standing, it is not clear whether
these organizations have enough sway to get the attention of a large percentage of
scientists around the world. To succeed in developing research integrity standards with
global impact, the ORI, ESF and OECD may need to partner with some other organizations
that have some influence on scientific ethics, such as the WMA, the United Nations
Educational, Scientific, and Cultural Organization (UNESCO), and professional associations,
such as the American Association for the Advancement of Science, German Association for
the Advancement of Science and Medicine, the Japanese Society for the Promotion of
Science, and so on. Scientists from all parts of the globe should be involved in developing
the standards.
The formation of an international society for ethics in research could be instrumental in
promoting international standards of research ethics. Currently, there is no such
organization. There are some international organizations, such as the ICMJE, COPE, WMA,
the International Conference on Harmonization (ICH, 2009), and the International
Association of Bioethics (IAB, 2009), that promote ethics in publication and human subjects
research, but there is no organization whose main focus is ethics in all aspects of research.
Another difficulty to overcome is that there are bound to be controversies concerning the
content of the international standards. Consider, for example, the definition of research
misconduct. Different countries have different definitions of research misconduct. The U.S.
federal government defines research misconduct as fabrication, falsification or plagiarism
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(FFP) (OSTP, 2000). Other countries, however, have definitions of misconduct that include
categories of behavior other than FFP. Norway defines misconduct as FFP as well as other
serious breaches of good scientific practice (Norwegian National Committee for Research
Ethics in Science and Technology, 2006). Finland distinguishes between fraud, which is
defined as FFP, and research misconduct, which is defined as gross negligence and
irresponsibility in the conduct of research (Finland, National Advisory Board on Research
Ethics, 2002). China's Ministry of Science and Technology has adopted a definition of
research misconduct that includes FFP as well as submitting false résumés and serious
violations of rules protecting human or animal research subjects (Chong, 2006). Australia's
definition of research misconduct includes FFP as well as failure to declare a serious conflict
of interest, serious violations of rules pertaining to research with human or animal research
subjects, and concealment of others' misconduct (Australian Research Council, 2007).
The most vexing issue in drafting an international definition of research misconduct may be
deciding whether the definition should include behaviors other than FFP (often referred to as
“fraud”), such as serious violations of rules protecting human or animal research subjects,
or serious departures from good scientific practice. For over a decade, policymakers in the
U.S. debated about the federal definition of research misconduct. In 1987, the Public Health
Service (PHS) and the National Science Foundation (NSF) defined misconduct as FFP as well
as other practices that deviate seriously from those commonly accepted in the scientific
community. The “other practices” category proved to be very controversial because it was
too general and vague. Two separate committees tried to resolve this controversy. Finally,
the Office of Science and Technology Policy (OSTP) proposed a narrower definition (i.e.,
misconduct = FFP), which has been adopted by various federal agencies, including the PHS
and NSF (Resnik, 2003). A debate similar to one that took place within the U.S. federal
government could be repeated at the international level if there is substantial support for
including behaviors other than FFP in the definition of misconduct.
Controversies may also arise concerning financial conflict of interest (COI) standards.
Although most researchers and policymakers agree on the importance of disclosing financial
interests, there is less agreement concerning whether to require anything beyond
disclosure, such as conflict management or prohibition, in some situations. In the U.S.,
funding agencies only require grant recipients to disclose financial interests; they do not
prohibit any types of financial interests. U.S. funding agencies also do not have any policies
concerning institutional COIs (Shamoo and Resnik, 2009). There is considerable variation
among university COI policies in the U.S. Though most universities require disclosure of
financial interests, few actually prohibit any types of financial relationships (McCrary et al.,
2000). Most medical schools have COI policies that pertain to institutional officials, but few
have policies that address financial interests held by the institution (Eringhaus et al., 2008).
In the U.S., the National Institutes of Health (NIH) intramural program has some of
strongest COI rules of any research organization. The NIH prohibits intramural investigators
from consulting with pharmaceutical and biotechnology companies and places limits on
stock ownership (NIH, 2008).
There is also likely to be some disagreement about whether international research integrity
standards should address the topic of social responsibility, i.e., promoting good
consequences for society and avoiding harmful ones. Some of the most important ethical
questions in scientific research, such as becoming involved in research related to national
defense or advocating for political causes, have to do with social responsibility (Shamoo and
Resnik, 2009). Many professional organizations, such as the American Anthropological
Association (1998), American Chemical Society (2007), American Physical Society (2002),
and American Society of Microbiology (2005), have codes of ethics that discuss the social
responsibilities of researchers. Several prominent books on research ethics also discuss the
social responsibilities of scientists (Shrader-Frechette, 1994; Resnik, 1998; Whitbeck,
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1998). However, the ethics standards promulgated by U.S. funding agencies do not mention
social responsibilities (Shamoo and Resnik, 2009). The guidelines developed by COPE
(2009) and ICMJE (2008) also do not mention social responsibility. The Office of Research
Integrity (ORI), which is responsible for promoting ethical standards in NIH-supported
research, has designated nine core areas for research ethics education, none of which
include social responsibility (ORI, 2006). ORI's Introduction to the Responsible Conduct of
Research, written by Nicholas Steneck, covers ORI's nine core areas but has no discussion
of social responsibility (Steneck, 2007).
One reason there may be some controversy about including social responsibility in
international research integrity standards is that honoring this ethical obligation often
requires researchers to reach beyond the familiar territory of the laboratory or research
group and apply their expertise to contentious social or political issues, such as
environmental protection, global warming, overpopulation, nuclear weapons, food and drug
safety, gun control, and so on. Some famous scientists who have taken their responsibilities
seriously have become embroiled in social and political controversy. For example, Rachel
Carson (1962) alerted the world to the dangers of pesticides, especially DDT, and helped to
launch the modern environmental movement when she published Silent Spring in 1962.
Although many people now regard Carson as the paragon of a socially responsible scientist,
at the time her book was published she was attacked by the chemical industry and the U.S.
Department of Agriculture and derided as a hysterical kook (Lear, 2009). Representatives
from diverse nations may decide to not articulate ethical standards related to social
responsibility, to prevent their deliberations from becoming bogged down in controversies
unrelated to the everyday conduct of science.
Once the sponsoring organizations reach some agreement on international research
integrity standards, the remaining problem is how to publicize and promote them. There is
little point in having an international research integrity code in name only: a code should be
a living document that influences the practice of science. The Nuremberg Code and Helsinki
Declaration, for example, have had considerable influence over the conduct of research with
human subjects. These two codes figure prominently in educational materials and scholarly
works on research with human subjects, government reports, journal policies, and even
legal opinions (Shamoo and Resnik, 2009; Brody, 1998; National Bioethics Advisory
Commission, 2001; Resnik, 2004; ICMJE, 2008). To ensure that an international code of
research integrity standards has significant influence, the groups promulgating the code
should consider partnering with scientific and professional organizations in various
countries, government agencies, journals, universities and others with an interest in
research integrity. Ideally, a partnership with organizations in different countries should be
formed before the ethical standards are adopted, so that instruments necessary for
publicizing and promoting the standard would already be in place.
The development of international standards of research integrity is clearly an idea whose
time has come. In fact, international standards of research integrity are long overdue.
Hopefully, some of the practical difficulties with advancing these standards will be overcome
soon, so that scientists will have guidelines for international research.
Acknowledgments
This research was sponsored by the intramural program of the National Institute of
Environmental Health Sciences (NIEHS), National Institutes of Health (NIH). It does not
represent the views of the NIEHS, NIH or U.S. government.
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Author
Address correspondence to Robin Pierce, J.D., Ph.D., Novel Tech Ethics, Dalhousie
University, 1234 LeMerchant Street, Halifax, Nova Scotia, B3H 3P7, Canada. E-mail:
pierce7@post.harvard.edu
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Background Even though research integrity (RI) training programs have been developed in the last decades, it is argued that current training practices are not always able to increase RI-related awareness within the scientific community. Defining and understanding the capacities and lacunas of existing RI training are becoming extremely important for developing up-to-date educational practices to tackle present-day challenges. Recommendations on how to implement RI education have been primarily made by selected people with specific RI-related expertise. Those recommendations were developed mainly without consulting a broader audience with no specific RI expertise. Moreover, the academic literature lacks qualitative studies on RI training practices. For these reasons, performing in-depth focus groups with non-RI expert stakeholders are of a primary necessity to understand and outline how RI education should be implemented. Methods In this qualitative analysis, different focus groups were conducted to examine stakeholders’ perspectives on RI training practices. Five stakeholders' groups, namely publishers and peer reviewers, researchers on RI, RI trainers, PhDs and postdoctoral researchers, and research administrators working within academia, have been identified to have a broader overview of state of the art. Results A total of 39 participants participated in five focus group sessions. Eight training-related themes were highlighted during the focus group discussions. The training goals, timing and frequency, customisation, format and teaching approach, mentoring, compulsoriness, certification and evaluation, and RI-related responsibilities were discussed. Although confirming what was already proposed by research integrity experts in terms of timing, frequency, duration, and target audience in organising RI education, participants proposed other possible implementations strategies concerning the teaching approach, researchers' obligations, and development an evaluation-certification system. Conclusions This research aims to be a starting point for a better understanding of necessary, definitive, and consistent ways of structuring RI education. The research gives an overview of what has to be considered needed in planning RI training sessions regarding objectives, organisation, and teaching approach.
... Among research ethicists, this is a broadly familiar argument, not only in stories about the origins and development of the field, but also in advocacy for better regulation, codification, or cooperation. It is not uncommon, for instance, to find authors bolstering their case for codification or implementation of research integrity standards with examples like Woo-Suk Hwang, the fraudulent South Korean stem cell researcher (Resnik 2009;Bouter 2020). Likewise, the Inter Academy Partnership cites the 'emergence of high-profile cases' like Hwang's as clear evidence of a need for global codification of ethical standards (Inter Academies 2012). ...
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... This research considered various ethical standards that were required while carrying out research. Shamoo and Resnik (2009) asserted that there was need to abide by the expected ethical standards while conducting research even when the research was being conducted by government agencies, professional bodies, or universities which have all embraced certain rules, codes, and policies that relate to research ethics. This research observed expected the ethical guidelines. ...
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... The penalties for scientific misconduct cover a wide range, and differences are seen at the international level. [75][76][77][78] International standards for research integrity are proposed, [79] and policies and initiatives addressing research misconduct have been prepared. [80] The penalty depends on whether the one involved is a student (undergraduate or postgraduate), a researcher or a laboratory technician, or a faculty or a staff member [ Table 6]. ...
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